Patterns of Evolution in the Feeding Mechanism of Actinopterygian Fishes1

Home , Ambloplites, Ductor, Luciocephalus pulcher, Neoteleostei, Operculum (fish), Pharyngeal jaw

AMER. ZOOL., 22:275-285 (1982)

GEORGE V. LAUDER Department of Anatomy, University of Chicago, Chicago, Illinois 60637

SYNOPSIS. Structural and functional patterns in the evolution of the actinopterygian feeding mechanism are discussed in the context of the major monophyletic lineages of ray-finned fishes. A tripartite adductor mandibulae contained in a maxillary-palatoquadrate chamber and a single mechanism of mandibular depression mediated by the obliquus inferioris, sternohyoideus, and hyoid apparatus are primitive features of the Actinopte- rygii. Halecostome fishes are characterized by having an additional mechanism of mandibular depression, the levator operculi—opercular series coupling, and a maxilla which swings anteriorly during prey capture. These innovations provide the basis for feeding by inertial suction which is the dominant mode of prey capture throughout the halecostome radiation. A remarkably consistent kinematic profile occurs in all suction-feeding halecostomes. Teleost fishes possess a number of specializations in the front jaws including a geniohyoideus muscle, loss of the primitive suborbital adductor component, and a mobile premaxilla. Structural innovations in teleost pharyngeal jaws include fusion of the dermal tooth plates with endoskeletal gill arch elements, the occurrence of a pharyngeal retractor muscle, and a shift in the origin of the pharyngohyoideus. These specializations relate to increased functional versatility of the pharyngeal jaw apparatus as demonstrated by an electromyographic study of pharyngeal muscle activity in Esox and Ambloplites. The major feature of the evolution of the actinopterygian feeding mechanism is the increase in structural complexity in both the pharyngeal and front jaws. Structural diversification is a function of the number of independent biomechanical pathways governing movement.

INTRODUCTION and function in fishes and in the proposal The evolution of the feeding mechanism and testing of functional explanations for in ray-finned fishes (Actinopterygii) pro- structure (Alexander, 1966, 1967, 1970; vides perhaps the best documented ex- Anker, 1974; Lauder, 1979; Liem, 1970; ample in the Vertebrata of change in a Osse, 1969). Functional analysis has be- structurally and functionally complex sys- come increasingly sophisticated and tech- tem. In the twenty years since the last re- niques such as high-speed cinematography view of the evolution of the feeding mech- (Elshoud-Oldenhave and Osse, 1976; Gro- anism in ray-finned fishes (Schaeffer and becker and Pietsch, 1979; Nyberg, 1971), Rosen, 1961), knowledge of both the his- electromyography (Ballintijn et al., 1972; torical pattern of diversification and the Lauder, 1980a; Liem, 1973; Liem and relation between structure and function Osse, 1975; Vandewalle, 1979), strain has increased tremendously. Phylogenetic gauges (Lauder and Lanyon, 1980), and analyses of actinopterygian evolutionary pressure transducers (Alexander, 1970; patterns have provided an excellent base- Lauder, 19806, c; Osse and Muller, 1981) line of information on the historical se- have largely obviated the need to base quence of structural change (Greenwood functional considerations on manipula- et al., 1966, 1973; Patterson, 1977, 1982; tions of preserved or freshly dead speci- Patterson and Rosen, 1977; Rosen, 1982), mens. As a result, many hypotheses about and as the discipline of experimental func- the functional significance of morpholog- tional morphology has developed, a cor- ical features in the actinopterygian skull responding increase has occurred in the have been tested, and many previously un- analysis of the relationship between form suspected relationships have emerged. In this paper, I will focus on structural and functional specializations in the evo- 1 From the Symposium on Evolutionary Morphology lution of the actinopterygian feeding of the Actinopterygian Fishes presented at the Annual Meeting of the American Society of Zoologists, 27- mechanism as they are reflected in nested 30 December 1980, at Seattle, Washington. sets of monophyletic lineages. I will em- 275 276 GEORGE V. LAUDER

HVOID

FIG. 2. Reconstruction of the superficial lateral (A) and ventral (B) cranial musculature in the paleonis- ciform fish Moythomasia nilida Gross. Osteological elements modified after Jessen (1968). The anterior branchiostegal rays have been removed in the ventral view to show the reconstructed throat musculature, and the maxilla in the lateral view has been partially removed to reveal the adductor musculature. The paired sternohyoideus muscles lie deep to the intermandibularis posterior and interhyoideus and are not FIG. 1. Structural network in the head of a primitive visible in this view. This reconstruction results from actinopterygian (A), a primitive halecostome (B), and deducing the most parsimonious primitive arrange- a percomorph (C) to show the biomechanical path- ment of adductor muscle character states in living ways governing mouth opening, suction feeding, and actinopterygians. Abbreviations: AMa, anterior (sub- jaw protrusion functions. Homologous biomechanical orbital) division of the adductor mandibulae; AMm, pathways are similarly numbered. Note the increase medial adductor division; AMp, posterolateral ad- in complexity of the structural network in actinop- ductor division; BM, branchiomandibularis muscle; terygian evolution. Only the function of jaw protru- CL, cleithrum; CLAV, clavicle; EP, epaxialis; IH, sion is shown in (C); the primitive functions of mouth interhyoideus; IMp, intermandibularis posterior opening and suction feeding are omitted for clarity. muscle; IO, infraorbital bone; MD, mandible; MX, Solid rectangles = bony elements; dashed rectan- maxilla; OBI, obliquus inferioris; OBS, obliquus gles = ligaments; parallelograms = muscles. Arrows superioris; OP, operculum; POP, preoperculum. run from the muscle to the bone of insertion; double- headed arrows indicate ligamentous connections between bony elements. Three dimensional rectangles indicate major functions which are realized (r, ar- adductor operculi muscle; EM, epaxial muscles; HY, rows) by the biomechanical couplings indicated. This hypaxial (obliquus inferioris) musculature; IHL, in- figure is not the same as the diagrams depicting the teroperculohyoid ligament; IML, interoperculoman- pattern of interrelationships and functional influ- dibular ligament; LAP, levator arcus palatini muscle; ences (see Dullemeijer, 1974, Fig. 62). Abbreviations: LOP, levator operculi muscle; MHL, mandibulohyoid AMI, division Al of the adductor mandibulae: A OP, ligament; SH. sternohvoideus muscle. FEEDING MECHANISMS IN RAY-FINNED FISHES 277

phasize characteristic features of the Ac- surface of the branchiostegal rays to insert tinopterygii, Halecostomi, Teleostei, Neo- in the fascia dorsal to the intermandibu- teleostei, and Percomorpha with the goal laris posterior. The hyohyoideus muscu- of suggesting certain general propositions lature of halecostomes appears to be de- about the nature of change in structural rived from the interhyoideus muscle fibers and functional networks within lineages of primitive actinopterygians (Fig. 2B: (also see Lauder, 1981). IH). The skull of primitive actinopterygians PRIMITIVE FEATURES OF THE possesses only a few mobile elements (Blot, ACTINOPTERYGIAN FEEDING MECHANISM 1978; Saint-Seine, 1956). The maxilla and Mouth opening in primitive actinopte- premaxilla are firmly attached to the other rygians is mediated by two musculoskeletal dermal skull bones and the opercle, sub- couplings (Figs. 1A, 2): the epaxial mus- opercle, and branchiostegal rays have lim- cles—neurocranium coupling which ele- ited lateral mobility. The oblique angle of vates the head (Fig. 1A: coupling 2), and the suspensory apparatus (reflected by the a ventral coupling involving the hypaxial position of the preoperculum, Fig. 2A: musculature, cleithrum, sternohyoideus, POP), results in a distinctly postorbital jaw and hyoid apparatus (Fig. 1A: coupling 1) articulation and limited lateral expansion. which causes mandibular depression. The three adductor mandibulae divisions Depression of the lower jaw is effected by are contained in a postorbital maxillary- retraction of the hyoid apparatus (by the palatoquadrate chamber. sternohyoideus and obliquus inferioris The experimental study of prey capture muscles) which exerts a posterodorsal in the primitive living actinopterygians Po- force on the mandible via the mandibulo- lypterus and Lepisosteus (Lauder, 1980a; hyoid ligament (Fig. 1A: MHL). This pos- Lauder and Norton, 1980) has revealed terodorsal force is applied at the insertion the importance of synchronous activity in of the mandibulohyoid ligament ventral to the obliquus inferioris and sternohyoideus the quadratomandibular articulation and muscles for mouth opening. The ventral thus causes mandibular depression (also division of the hypaxialis (=obliquus infer- see Lauder, 1980a, Fig. 18; 1980d)- This ioris) stabilizes the pectoral girdle so that mechanism of mandibular depression is the primary effect of the sternohyoideus also found in lungfishes, coelacanths, and is to cause posteroventral hyoid rotation, sharks and is thus primitive for the Tel- thus opening the mouth. Experimental eostomi. analysis reveals no evidence for the pos- A reconstruction of the jaw musculature terior movement of the pectoral girdle in a palaeoniscoid is illustrated in Figure which has been suggested to be involved 2. Laterally, the adductor mandibulae is in feeding (Hutchinson, 1973; Schaeffer divided into three divisions: an anterior and Rosen, 1961; Tchernavin, 1953). The (suborbital) division, a medial division, and ventral throat musculature plays little role a posterolateral division (Fig. 2A). These in mediating mouth opening. The inter- three adductor components are hypothe- mandibularis posterior, interhyoideus, and sized to be homologous with similarly lo- branchiomandibularis (Fig. 2B) are pri- cated muscle divisions in Polypterus, Lepi- marily active during chewing and intraoral sosteus, and Amia (see Lauder [1980a, e] for manipulation of prey items, and may be a more extensive discussion of muscle ho- used to control fluid flow through the oral mologies). An intramandibular adductor cavity. These ventral muscles are not in- (Aw) occupies the mandibular adductor volved in opening the mouth. fossa. Ventrally, the paired sternohyoideus Primitive actinopterygian fishes (e.g., muscles extend anteriorly to insert on the Cheirolepis, Moythomasia) possessed a cephalic urohyal. A flat, wide intermandibularis musculoskeletal system which is consider- posterior spans the mandibular rami (Fig. ably less complex mechanically than that 2B: IMp) and the interhyoideus extends of the Halecostomi. There were relatively anteriorly from the ceratohyal and dorsal few mobile elements in the skull and ex- 278 GEORGE V. LAUDER

pansion of mouth cavity volume during control of fluid flow and suction feeding. feeding was probably quite small due to The maxilla, primitively firmly attached to the limited lateral mobility of the suspen- the neurocranium and forming the lateral sorium, opercle, and branchiostegal ele- wall of the adductor chamber (Fig. 2A; ments. Water flow through the mouth cav- Gardiner, 1963; Schaeffer and Rosen, ity during feeding may thus have been 1961) is free from the cheek and pivots on primarily controlled by body velocity, and a medially directed process posterior to the not by movement of skull elements. vomer. High-speed cinematography of prey capture by Amia calva and several THE HALECOSTOME FEEDING MECHANISM primitive teleosts (Lauder, 1979) has re- The Halecostomi share two major struc- vealed that the maxilla swings anteriorly tural innovations related to the feeding on its neurocranial pivot as the mouth mechanism and possess a network of struc- opens, and by preventing fluid inflow tural connections in the head which is con- through the corners of the mouth, results siderably more complex than that of the in anteroposteriorly oriented streamlines paleoniscoid fishes (Fig. IB). Halecostome which increase the velocity of water move- fishes share two independent biomechan- ment from in front of the mouth into the ical pathways mediating lower jaw depres- oral cavity (see Fig. 3A: MX). Secondly, an sion: the primitive coupling involving the increase in the volume change within the hypaxial musculature, pectoral girdle, orobranchial cavity results both from the sternohyoideus, and hyoid apparatus (Fig. vertical orientation of the suspensorium IB: coupling 1), and a second, new cou- and from increased ventral mouth cavity pling involving the opercular apparatus expansion as a result of a greater range of (Fig. IB: coupling 2). This opercular series hyoid depression. A mobile maxilla, poten- coupling is retained in nearly all of the tially large orobranchial volume changes, 25,000 species of halecostomes and is a re- and increased kinematic versatility, are markably persistent component of the features which are maintained in suction structural network of the head. feeding fishes throughout the halecostome Mandibular depression by levation of radiation. the operculum is accomplished by contrac- The kinematic pattern which is charac- tion of the levator operculi muscle which teristic of primitive halecostome fishes is is derived from the adductor operculi of also maintained in all generalized preda- primitive actinopterygians (Fig. 1A, B: ceous fishes studied to date (Figs. 3, 4). As AOP, LOP). The levator operculi causes a the mouth begins to open during feeding, dorsal rotation of the opercular series the operculum and branchiostegal rays are (opercle, subopercle, and interopercle) adducted against the pectoral girdle (Fig. which is applied as a posterodorsal force 3B: frames 1 and 2), preventing water in- on the mandible via the interoperculoman- flow. Maxillary swing and opercular leva- dibular ligament (Fig. IB: IML). Both the tion reach a peak nearly synchronously levator operculi and interoperculum rep- with peak mouth opening which is fol- resent structural specializations at the hal- lowed by hyoid depression and opercular ecostome level. The consequence of hav- dilation. The mouth then rapidly closes ing two biomechanically independent while hyoid depression, suspensorial ab- pathways mediating mandibular depres- duction, and opercular dilation return to sion is a dissociation of the primitive hyoid their initial positions (Figs. 3, 4). The pro- coupling (Fig. 1A, B: coupling 1) from cess of buccal compression thus involves a obligatory mouth opening functions. This sequence of movement different from allows changes in the timing of hyoid mouth cavity expansion. depression in relation to mouth opening Patterson (1973) considers the extinct and increases the versatility of control of groups Parasemionotidae and Semionoti- fluid movement through the oral cavity. dae to represent primitive grades of hale- Primitive halecostomes possess two oth- costome organization. Both groups in- er structural innovations which relate to clude forms which show the structural FEEDING MECHANISMS IN RAY-FINNED FISHES 279

OPERCULAR DILATION (cm)

LOWER JAW ANGLE (degrees)

ANGLE OF MAXILLA (degrees)

1 3 5 7 9 11 13 15 17 19 21 23 FRAME NUMBER (TIME) ^^

FIG. 3. Prey capture in Atnia calva as seen in lateral FIG. 4. Pattern of jaw bone movement in Salvelmus (A) and ventral (B) views. This figure is traced from fontinalts to illustrate the primitive halecostome ki- frames of high-speed films of two separate prey cap- nematic profile. The relative sequence of bone move- ture events. (Modified from figures 13 and 14 of Lau- ment at the strike is very similar in all predaceous der [1980a].) Note the delay in opercular and bran- halecostomes that have been studied experimentally chiostegal expansion until the mouth is nearly (see text). completely open, and the anteropostenor sequence of peak excursion in mouth opening, hyoid depression, and opercular dilation. Abbrevations: GP, gular plate; MX, maxilla. a medial portion which becomes associated with the ethmoid complex (Patterson, 1973). In a number of predaceous teleosts correlates of a suction feeding mechanism. {e.g., Hoplias, Salmo) the premaxilla has be- For example, Lepidotes has a well-devel- come secondarily firmly attached to the oped interopercle and a free maxilla bear- neurocranium, but the primitive condition ing a prominent medial process (personal for teleosts as exemplified by Pholidopho- observation on MCZ 5304, Lepidotes elven- rus, Leptolepis, or ichthyodectiforms, is a sis). The hyoid apparatus of Lepidotes also small mobile premaxilla (Patterson, 1977; appears to be very similar to that of other Patterson and Rosen, 1977). halecostomes. Although there have been major modifications within the Teleostei in the overall THE TELEOST FEEDING MECHANISM shape of the jaw and its component ele- Major structural features ments, only three major types of change The teleost feeding mechanism is distin- have occurred in the pattern of intercon- guished from that of more primitive hal- nections in the structural network, of the ecostomes by the division of the premaxilla head. The first specialization involves a into a mobile lateral toothed portion and shift in insertion of the mandibulohyoid 280 GEORGE V. LAUDER

ligament to the interoperculum (Fig. 1C: and Weitzman, 1982; Rosen, 1973). In IHL). The interoperculohyoid ligament many other lineages, a lateral subdivision characterizes the feeding mechanism of of A2/3, Al, inserts tendinously on the eurypterygian fishes (=Aulopiformes + maxilla. Based on the diversity of lineages Myctophiformes + Paracanthopterygii + within the Acanthopterygii which possess Acanthopterygii; Rosen, 1973) and effec- a so-called Al adductor division, it is un- tively shifts the action of the hyoid and likely that this division is homologous opercular coupling onto the interopercul- throughout advanced teleosts, and mus- um. Only the interoperculomandibular cular attachments to the maxilla have cer- ligament transmits posterodorsal hyoid and tainly arisen independently in various opercular movement to the mandible in the more primitive teleostean lineages. A Eurypterygii, while other teleosts retain number of percomorph lineages have a the primitive two-coupling system of subdivided main adductor mass with sep- halecostomes (Fig. IB). arate A2 and A3 components. The A3 usu- The second major structural specializa- ally inserts on the coronomeckelian bone tion within teleosts is the development of in the Meckelian fossa, while A2 may insert an elongate ascending process on the pre- along the coronoid process and medial maxilla and modification of maxillary and face of the dentary and anguloarticular. A premaxillary articular surfaces and liga- well-developed intramandibular adductor ments, all associated with protrusion of the division (Aw) is present in most teleosts. upper jaw toward the prey during feeding (Fig- 1). Models and mechanisms of upper jaw Finally, a number of changes in the jaw protrusion: The Acanthopterygii adductor musculature have occurred. The ability of many acanthopterygians Primitive teleosts are characterized by the to extend the premaxilla and maxilla to- presence of a geniohyoideus muscle ex- ward the prey during feeding (protrusion) tending anteroposteriorly between the is one of the most widely discussed fea- mandibular symphysis and the ceratohyal tures of the teleost feeding mechanism and epihyal. The geniohyoideus muscle of (Alexander, 1967; Eaton, 1935; Gregory, teleosts represents a fused intermandibu- 1933; Lauder and Liem, 1981; Liem, laris posterior and interhyoideus (Fig. 2) 1970, 1979, 1980; Nyberg, 1971; Pietsch, of primitive actinopterygians (Winterbot- 1978; Schaeffer and Rosen, 1961; van tom, 1974). Teleosts have lost the bran- Dobben, 1937). It is now clear that acan- chiomandibularis of primitive actinopte- thopterygians possess a number of differ- rygians (Lauder, 1980a; Wiley, 1979), as ent mechanisms of protrusion involving well as the suborbital adductor component non-homologous articular surfaces, liga- (Fig. 2A: AMa). Only a single unsubdivid- ments, and possibly also muscular control ed lateral adductor muscle is present in mechanisms. primitive members of the Osteoglossomor- Alexander (1967) has provided a me- pha, Elopomorpha, and Clupeomorpha, chanical explanation for premaxillary pro- whereas in many euteleostean lineages trusion which seems to apply to some both lateral and medial subdivisions of the primitive acanthopterygians. He suggested main adductor mass (A2/3—Winterbot- that rotation of the maxilla along its long tom, 1974) are present. Of particular im- axis is caused by depression of the lower portance for the evolution of protrusile jaw and contraction of the A1 division of mechanisms in teleosts is the independent the adductor mandibulae. Maxillary rota- evolution in many lineages of one or more tion causes the premaxillary process of the adductor divisions with insertions on the maxilla to press against the articular pro- maxilla. Stomiiforms, myctophiforms, some cess of the premaxilla which forces the paracanthopterygians, and some primitive premaxilla to protrude anteriorly. The two acanthopterygian fishes possess a medial prerequisites for this mechanism are (1) subdivision of the main adductor mass. maxillary twisting and (2) apposition of the Alb, which inserts on the maxilla (Fink premaxillarv articular surface with the FEEDING MECHANISMS IN RAY-FINNED FISHES 281 premaxillary condyle of the maxilla. Alex- protrusion actually increases the success of ander (1967) also noted that movements of prey capture, and how jaw protrusion ef- the suspensory apparatus may limit retrac- fects the hydrodynamic properties of the tion of the protruded premaxilla. Suspen- feeding mechanism. sory abduction causes the maxillary process of the palatine to move medially and Pharyngeal jaw evolution block retraction which can only be accom- Upper pharyngeal jaw dentition in plished with an adducted suspensorium. primitive actinopterygians consists of nu- Thus suspensorial, maxillary, and premax- merous dermal tooth plates aligned with illary movements are all coupled with ki- (but not fused to) the pharyngobranchial nematic systems involved in mouth open- and epibranchial gill arch elements. Amia ing, and mandibular depression ultimately and Lepisosteus are unique among non-te- controls protrusion (Liem, 1970). leost actinopterygians in having many Liem (1979, 1980) has proposed a "de- small tooth plates grouped into a large coupled model" for cichlid fishes which posterior patch so that individual tooth lack the requisite anatomical articulations plates are not referable to a particular arch for Alexander's (1967) model. This model (Nelson, 1969). Ventrally, small dermal involves contraction of the epaxial muscles tooth plates are aligned with a long and and concomitant stabilization of the pre- slender fifth ceratobranchial (Nelson, maxilla, maxilla, and mandible by contrac- 1969; Nielsen, 1942). These plates become tion of the adductor mandibulae (parts Al closely associated in Amia, Lepisosteus, Hio- and/or A2) and geniohyoideus. By lifting don, and Elops but are not fused to the fifth the neurocranium, jaw protrusion can be ceratobranchial. modulated and varied in relation to the In the Teleostei, upper pharyngeal den- degree of synchronous activity in the ge- tition is consolidated into one to five paired niohyoideus and adductor mandibulae. Ex- tooth plates (Nelson, 1969). Clupeo- perimental analysis of prey manipulation morphs and euteleostean fishes (the Clu- in cichlids (Liem, 1979, 1980) shows that peocephala, Patterson and Rosen, 1977) the epaxial musculature is involved in are derived in having the upper pharyn- modulating upper jaw movement during geal tooth plates fused to the bony endo- manipulation of prey and that the decou- skeletal gill arch elements, and a single pled protrusion system allows complex ki- large tooth plate fused to ceratobranchial nematic patterns of jaw movement not five. In many euteleostean lineages, only seen in fishes with coupled mechanisms. one or two large toothplates are present in A number of functions have been pro- the upper pharyngeal dentition (Nelson, posed for premaxillary protrusion, but few 1969, p. 492), and pharyngobranchial one of these hypotheses have been tested ex- commonly serves as the suspensory ele- perimentally. Protrusion may be related to ment of the gill basket (see Fig. 5). bottom feeding by allowing the mouth A particularly important specialization opening to be pointed ventrally while the during higher teleostean evolution, and predator's body remains horizontal (Alex- one which characterizes the Neoteleostei ander, 1966, 1967). For mid water suction (Rosen, 1973), is the occurrence of a re- feeding, Nyberg (1971), Gosline (1971), tractor dorsalis muscle. The retractor dor- and Alexander (1967) have hypothesized salis (=retractor arcus branchialium) is a that protrusion provides an added velocity paired muscle which originates on the ver- component to the predator's approach. tebral column (anywhere from the first to Nyberg (1971) measured an "added veloc- the sixteenth vertebra) and extends an- ity" of 89% of the average attack velocity teroventrally to insert mainly on pharyn- in Micropterus, and Lauder and Liem gobranchials three and four (Rosen, 1973; (1981) measured an additional velocity of Fig. 5B: RD). A second important inno- 39% of average attack velocity in Lucio- vation is the shift in origin of the pharyn- cephalus. It remains to be demonstrated gohyoideus muscle (Fig. 5: PH), which whether the added velocity resulting from primitively originates on ventral gill arch 282 GEORGE V. LAUDER

specializations is the presence in higher euteleosts of mechanical couplings which increase the versatility of the pharyngeal ESOX apparatus. In primitive teleosts (Fig. 5), protraction and retraction of the upper pharyngeal tooth plates must be accomplished by the levator externus muscles. Levator externus one (and the anterior levator interni) have a posteriorly inclined line of action which results in retraction of the upper pharyngeal jaw (Fig. 5A: LEI). Levator externi two and three mediate upper pharyngeal jaw protraction. In higher euteleosts (Fig. 5B), the retractor dorsalis and antagonistic levator externi three and four provide a coupling which allows extensive anteroposterior movement of the upper pharyngeal jaws. In addition, the levator posterior mediates dorsal movement of the upper jaws. Ventrally, the change in origin of the pharyngohyoideus (Fig. 5B) to the urohyal increases the range of anterior movement of the lower pharyngeal jaw, and, in con- junction with the pharyngocleithralis internus, provides a coupling mediating anteroposterior excursions. sins'* Experimental evidence from electromy- FIG. 5. Diagrammatic view of the pharyngeal jaws ographic analyses of pharyngeal muscula- and their relation to the skull in (A) Esox niger and ture in euteleosteans (Fig. 5) reflects these (B) Ambloplites rupestris. Heavy lines indicate pharyn- constraints on lower pharyngeal jaw move- geal jaw muscles and their approximate line of action. ment. In Esox, swallowing is accomplished Thin lines represent the branchial basket. Black bars represent electromyographic activity in selected bran- by synchronous activity in levator externus chial muscles during manipulation and deglutition; one and the pharyngocleithralis internus white bars indicate occasional activity. The short ver- (Fig. 5A: LEI, PCi) indicating that both the tical line anterior to levator externus one connects the upper and lower pharyngeal jaws are re- gill basket with the neurocranium and represents pharyngobranchial one. Note the two salient special- tracted together. After retraction, levator izations which distinguish advanced euteleosteans externus three is active, elevating and pro- such as Ambloplites from more primitive forms (Esox): tracting the upper pharyngeal jaw before (1) the shift in origin of the pharyngohyoideus muscle the second retraction stroke of the lower (PH) to the urohyal, and (2) the occurrence of a re- jaw. tractor dorsalis muscle (RD). Abbreviations: AD5, fifth branchial adductor; GH, geniohyoideus; LE1-4, In Ambloplites (Fig. 5B), the pharyngo- levator externi muscles; PCi, e, pharyngocleithralis hyoideus and geniohyoideus are active internus and externus muscles; PH, pharyngohyoi- synchronously to protract the lower pha- deus; RD, retractor dorsalis; SH, sternohyoideus. ryngeal jaw, while the upper jaw is being protracted by the levator externi muscles elements (usually hypobranchial three). In (Fig. 5B: LE4). Retraction of the upper jaw- all myctophiform, paracanthopterygian, occurs via the retractor dorsalis which is and acanthopterygian teleosts (Subsection active with the pharyngocleithralis inter- Ctenosquamata, Rosen, 1973) the pha- nus (Fig. 5B: RD, PCi). The upper and ryngohyoideus originates from the uro- lower jaws thus are retracted together, al- hyal (Fig. 5: PH). though the excursion of the lower jaw is The consequence of these two muscular onh one-half that of the upper jaw. FEEDING MECHANISMS IN RAY-FINNED FISHES 283

In certain acanthopterygian lineages, dochondral gill arch elements characterizes the lower pharyngeal jaws are fused in the the Clupeocephala; the presence of a re- midline and osteological and myological tractor dorsalis is shared by neoteleostean specializations of the entire pharyngeal ap- fishes; and the pharyngohyoideus muscle paratus result in radically different ki- originates from the urohyal in the Cteno- nematic and electromyographic patterns squamata. These anatomical specializa- from generalized euteleosts (Liem, 1973, tions result in increased control over prey 1978; Liem and Greenwood, 1981). manipulation and mastication in the phar- ynx and reflect the increasing functional CONCLUSIONS versatility of pharyngeal jaw elements in Considerable progress has been made actinopterygian evolution. over the last twenty years in understanding patterns of structural and functional evo- ACKNOWLEDGMENTS lution in the feeding mechanism of fishes, I gratefully acknowledge the Society of and actinopterygians provide an excellent Fellows, Harvard University, for a Junior case study for analyzing the nature and Fellowship during which this paper was pattern of structural changes in a complex prepared, and NSF DEB 80-03206 for system. In particular, an analysis of how travel support. Bill Fink, Sara Fink, and the structural network in the front jaws has Karel Liem kindly reviewed the manu- changed (Fig. 1) may be correlated with a script. Figure 2 was drawn by Sara Fink. similar analysis for pharyngeal jaw structural and functional systems (Fig. 5) to gain an understanding of evolutionary in- REFERENCES teractions between these two coupled Alexander, R. McN. 1966. The functions and mech- structural features. anisms of the protrusible upper jaws of two One of the major features of the evolu- species of cyprinid fish. J. Zool., London tion of the actinopterygian feeding mech- 149:288-296. anism is an increase in structural complex- Alexander, R. McN. 1967. The functions and mechanisms of the protrusible upper jaws of some ity. As more cladistically derived acanthopterygian fish. J. Zool., London 151:43- monophyletic lineages of actinopterygians 64. are considered, structural complexity (de- Alexander, R. McN. 1970. Mechanics of the feeding fined as the number of connections in the action of various teleost fishes. J. Zool., London structural network, Fig. 1) increases. Cer- 162:145-156. Anker, G. 1974. Morphology and kinetics of the tain changes in the structural network are head of the stickleback, Caiterosleia aculeatus. related to structural diversification. For ex- Trans. Zool. Soc. Lond. 32:311-416. ample, the occurrence of two biomechan- Ballintijn, C. M., A. van den Burg, and B P. Egber- ical pathways mediating jaw opening at the ink. 1972. An electromyographic study of the halecostome level permits structural and adductor mandibulae complex of a free-swim- ming carp (Cyprinus carpio) during feeding. J. functional diversification by removing Exp. Biol. 57:261-283. functional constraints on the primitive Blot, J. 1978. Origine et phylogenese des poissons hyoid coupling. A similar relationship be- osseux. Boll. Zool. 45:1-21 (Suppl. II). tween structural diversity and number of Dullemeijer, P 1974. Concepts and approaches in biomechanical pathways holds for mecha- animal morphology Van Gorcum, Assen, The Netherlands. nisms of jaw protrusion and upper jaw Eaton, T. H. 1935. Evolution of the upper jaw mech- morphology in acanthopterygians (Lau- anism in teleost fishes. J. Morph. 58:157-172. der, 1981). Elshoud-Oldenhave, M. J. W. 1979. Prey capture in the pike-perch, Stizostedion lucioperca (Teleostei, In the pharyngeal jaws, three major Percidae): A structural and functional analysis. structural and functional modifications Zoomorphologie 93:1-32. have occurred in teleosts and the distri- Elshoud-Oldenhave, M. J. W. and J. W. M. Osse. bution of these modifications is congruent 1976. Functional morphology of the feeding sys- with currently accepted monophyletic lin- tem in the ruff—Gymnocephalus cernua (L. 1758)— (Teleostei, Percidae). J. Morph. 150:399-422. eages. Consolidation and fusion of pha- Fink, W. L. and S. H. Weitzman. 1982. Relationships ryngeal tooth plates with underlying en- of the stomiiform fishes (Teleostei), with a de- 284 GEORGE V. LAUDER

scription of Diplophos. Bull. Mus. Comp. Zool. muscle activity during feeding in the gar, Lepi- 150:31-93. sosleus oculatus. J. Exp. Biol. 84:17-32. Gardiner, B. G. 1963. Certain palaeoniscoid fishes Liem, K. F. 1970. Comparative functional anatomy and the evolution of the snout in actinopte- of the Nandidae (Pisces: Teleostei). Fieldiana, rygians. Bull. Br. Mus. Nat. Hist. (Geol.) 8:255- Zoology 56:1—166. 325. Liem, K. F. 1973. Evolutionary strategies and mor- Gosline, W. A. 1971. Functional morphology and clas- phological innovations: Cichlid pharyngeal jaws. sification of teleostean fishes.Univ . Press of Hawaii, Syst. Zool. 22:425-441. Honolulu. Liem, K. F. 1978. Modulatory multiplicity in the Greenwood, P. H., D. E. Rosen, S. H. Weitzman, and functional repertoire of the feeding mechanism G. S. Myers. 1966. Phyletic studies of teleostean in cichlid fishes. I. Piscivores. J. Morph. 158:323- fishes, with a provisional classification of living 360. forms. Bull. Am. Mus. Nat. Hist. 131:339-456. Liem, K. F. 1979. Modulatory multiplicity in the Greenwood, P. H., R. S. Miles, and C. Patterson, feeding mechanism in cichlid fishes, as exempli- (eds.) 1973. Interrelationships of fishes. Academic fied by the invertebrate pickers of Lake Tangan- Press, London. yika. J. Zool., London 189:93-125. Gregory, W. K. 1933. Fish skulls. A study of the evo- Liem, K. F. 1980. Adaptive significance of intra- and lution of natural mechanisms. Trans. Amer. Phil. interspecific differences in the feeding reper- Soc. 23:75-481. toires of cichlid fishes. Amer. Zool. 20:295-314. Grobecker, D. B. and T. W. Pietsch. 1979. High- Liem, K. F. and P. H. Greenwood. 1981. A functional speed cinematographic evidence for ultrafast approach to the phylogeny of the pha- feeding in antennariid anglerfishes. Science ryngognath teleosts. Amer. Zool. 21:83—101. 205:1161-1162. Liem, K. F. and J. W. M. Osse. 1975. Biological ver- Hutchinson, P. 1973. A revision of the redfieldiiform satility, evolution, and food resource exploitation and perleidiform fishes from the Triassic of in African cichlid fishes. Amer. Zool. 15:427— Bekker's Kraal (South Africa) and Brookvale 454. (New South Wales). Bull. Br. Mus. Nat. Hist. Nelson, G. J. 1969. Gill arches and the phylogeny of Geol. 22:233-354. fishes, with notes on the classification of verte- Jessen, H. 1968. Moythomasia nitida Gross und M. cf brates. Bull. Am. Mus. Nat. Hist. 141:475-552. strtata Gross, Devonische Paleonisciden aus dem Nielsen, E. 1942. Studies on Triassic fishes from East Oberen Plattenkalk der Bergischen-Gladbach- Greenland. I. Glaucolepis and Boreosomus. Med. Paffrather Mulde (Rheinisches schiefergebirge). Gron. 138:1-394. Palaeontigraphica 128A:87-114. Nyberg, D. W. 1971. Prey capture in the largemouth Lauder, G. V. 1979. Feeding mechanisms in primi- bass. Amer. Midi. Nat. 86:128-144. tive teleosts and in the halecomorph fish Amia Osse, J. W. M. 1969. Functional morphology of the calva. J. Zool., London 187:543-578. head of the perch (Perca fluviatilisL.) : An elec- Lauder, G. V. 1980a. Evolution of the feeding mech- tromyographic study. Neth. J. Zool. 19:289-392. anism in primitive actinopterygian fishes: A Osse, J. W. M. and M. Muller. 1981. A model of functional anatomical analysis of Polypterus, Lep- suction feeding in teleostean fishes with some im- tsosteus, and Amia. J. Morph. 163:282-317. plications for ventilation. In M. A. Ali, (ed.), En- Lauder, G. V. 19804. Hydrodynamics of prey cap- vironmental physiology of fishes. Plenum Press, New ture by teleost fishes. In Biofiuid mechanics, Vol. York. 2, pp. 161-181. Plenum Press, N.Y. Patterson, C. 1973. Interrelationships of holosteans. Lauder, G. V. 1980f. The suction feeding mecha- In P. H. Greenwood, R. S. Miles, and C. Patter- nism in sunfishes (Lepomis): An experimental son (eds.), Interrelationships of fishes,pp . 233—305. analysis. J. Exp. Biol. 88:49-72. Academic Press, London. Lauder, G. V. 1980*. The role of the hyoid appa- Patterson, C. 1977. The contribution of paleontology ratus in the feeding mechanism of the coelacanth to teleostean phylogeny. In M. K. Hecht, P. C. Latimeria chalumnae. Copeia 1980:1-9. Goody, and B. M. Hecht, (eds.), Major patterns in Lauder, G. V. 1980f. On the evolution of the jaw vertebrate evolution, pp. 579-643. Plenum Press, adductor musculature in primitive gnathostome New York. fishes. Breviora 460:1-10. Patterson. C. 1982. Morphology and interrelation- Lauder, G. V. 1981. Form and function: Structural ships of primitive actinopterygian fishes. Amer. analysis in evolutionary morphology. Paleobiol- Zool. 22:241-259. ogy 7:430^142. Patterson, C. and D. E. Rosen. 1977. Review of ich- Lauder, G. V. and L. E. Lanyon. 1980. Functional thyodectiform and other Mesozoic teleost fishes anatomy of feeding in the bluegill sunfish, Le- and the theory and practice of classifying fossils. pomis macrochirus: In vivo measurement of bone Bull. Am. Mus. Nat. Hist. 158:81-172. strain. J. Exp. Biol. 84:33-55. Pietsch, T. W. 1978. The feeding mechanism of Sty- Lauder, G. V. and K. F. Liem. 1981. Prey capture by lephorus chordatus (Teleostei: Lampridiformes): Luciocephalus pulcher: Implications for models of Functional and ecological implications. Copeia jaw protrusion in teleost fishes. Env. Biol. Fish. 1978:255-262. 6:257-268. Rosen, D. E. 1973. Interrelationships of higher tu- I-auder. G V and S. F. Norton. 1980. As\mmetrKal teleostean fishes. In P. H. Greenwood, R. S. FEEDING MECHANISMS IN RAY-FINNED FISHES 285

Miles, and C. Patterson (eds.). Interrelationships of ismus der Knochenfishe. Arch. Neerl. Zool. 2:1- fishes, pp. 397—513. Academic Press, London. 72. Rosen, D. E. 1981. Teleostean interrelationships, Vandewalle, P. 1979. Etude cinematographique et morphological function and evolutionary infer- electromyographique des mouvements respira- ence. Amer. Zool. 22:261-273. toires chez trois cyprins, Gobto gobto (L.), Barbus Saint-Seine, P. 1956. L'evolution des actinoptery- barbus (L.) et Leuciscus leuciscus (L.). Cybium 6:3— giens. Coll. int. Paleont. CNRS Paris 60:27-33. 28. Schaeffer, B. and D. E. Rosen. 1961. Major adaptive Wiley, E. O. 1979. Ventral gill arch muscles and the levels in the evolution of the actinopterygian interrelationships of gnathostomes, with a new feeding mechanism. Amer. Zool. 1:187-204. classification of the vertebrata. Zool. J. Linn. Soc. Tchernavin, V. V. 1953. The feeding mechanisms of a 67:149-179. deep sea fish Chauliodus sloani Schneider. British Winterbottom, R. 1974. A descriptive synonymy of Museum, N. H., London. the striated muscles of the Teleostei. Proc. Acad. van Dobben, W. H. 1937. Uber den Kiefermechan- Nat. Sci. Phil. 125:225-317.